Phylogenetic conservatism in skulls and evolutionary lability in limbs - Morphological evolution across an ancient frog radiation is shaped by diet, locomotion and burrowing

Abstract

Background Quantifying morphological diversity across taxa can provide valuable insight into evolutionary processes, yet its complexities can make it difficult to identify appropriate units for evaluation. One of the challenges in this field is identifying the processes that drive morphological evolution, especially when accounting for shape diversification across multiple structures. Differential levels of co-varying phenotypic diversification can conceal selective pressures on traits due to morphological integration or modular shape evolution of different structures, where morphological evolution of different modules is explained either by co-variation between them or by independent evolution, respectively.

Methods Here we used a 3D geometric morphometric approach with x-ray micro CT scan data of the skull and bones of forelimbs and hindlimbs of representative species from all 21 genera of the ancient Australo-Papuan myobatrachid frogs and analysed their shape both as a set of distinct modules and as a multi-modular integrative structure. We then tested three main questions: (i) are evolutionary patterns and the amount and direction of morphological changes similar in different structures and subfamilies?, (ii) do skulls and limbs show different levels of integration?, and (iii) is morphological diversity of skulls and limbs shaped by diet, locomotion, burrowing behavior, and ecology?.

Results Our results in both skulls and limbs support a complex evolutionary pattern typical of an adaptive radiation with an early burst of phenotypic variation followed by slower rates of morphological change. Skull shape diversity was phylogenetically conserved and correlated with diet whereas limb shape was more labile and associated with diet, locomotion, and burrowing behaviour. Morphological changes between different limb bones were highly correlated, depicting high morphological integration. In contrast, overall limb and skull shape displayed semi-independence in morphological evolution, indicating modularity.

Conclusions Our results illustrate how morphological diversification in animal clades can follow complex processes, entailing selective pressures from the environment as well as multiple trait covariance with varying degrees of independence across different structures. We suggest that accurately quantifying shape diversity across multiple structures is crucial in order to understand complex evolutionary processes.